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Bat Coronavirus Phylogeography in the Western Indian Ocean bioRxiv preprint doi: https://doi.org/10.1101/742866; this version posted March 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Bat coronavirus phylogeography in the Western Indian Ocean 2 Léa Joffrin a#, Steven M. Goodman b, c, David A. Wilkinson a, Beza Ramasindrazana a, b*, Erwan 3 Lagadec a, Yann Gomard a, Gildas Le Minter a, Andréa Dos Santos d, M. Corrie Schoeman e, 4 Rajendraprasad Sookhareea f, Pablo Tortosa a, Simon Julienne g, Eduardo S. Gudo h, Patrick 5 Mavingui a and Camille Lebarbenchon a# 6 a Université de La Réunion, UMR Processus Infectieux en Milieu Insulaire Tropical (PIMIT), 7 INSERM 1187, CNRS 9192, IRD 249, Sainte-Clotilde, La Réunion, France. 8 b Association Vahatra, Antananarivo, Madagascar. 9 c Field Museum of Natural History, Chicago, USA. 10 d Veterinary Faculty, Eduardo Mondlane University, Maputo, Mozambique. 11 e School of Life Sciences, University of Kwa-Zulu Natal, Kwa-Zulu Natal, South Africa. 12 f National Parks and Conservation Service, Réduit, Mauritius. 13 g Seychelles Ministry of Health, Victoria, Mahe, Seychelles. 14 h Instituto Nacional de Saúde, Maputo, Mozambique. 15 16 Running head: Bat coronavirus in the Western Indian Ocean 17 18 #Corresponding authors: [email protected]; [email protected] 19 UMR PIMIT, 2 rue Maxime Rivière, 97490 Sainte-Clotilde, Reunion Island, France. 20 21 *Present address: Beza Ramasindrazana, Institut Pasteur de Madagascar, BP 1274, Amba- 22 tofotsikely, Antananarivo 101, Madagascar 23 24 Abstract word count: 171 Manuscript word count: 3158 1 bioRxiv preprint doi: https://doi.org/10.1101/742866; this version posted March 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 Author Contributions: CL and LJ conceived and designed the study. BR, CL, DAW, EL, LJ, 26 PT, SMG and YG collected biological material on Madagascar. SMG, RS and YG collected 27 biological material on Mauritius. BR, EL and GLM, collected biological material on Mayotte. 28 SMG, GLM, ADS and MCS, collected biological material in Mozambique. BR, DAW, EL and 29 GLM collected biological material on Reunion Island. EL, GLM, SJ and YG collected biolog- 30 ical material in the Seychelles. LJ performed the molecular analyses. CL, DAW, and LJ ana- 31 lyzed the data. CL and LJ wrote the paper. SMG, ESG, PM and SJ contributed to the project 32 management in Malagasy, Mauritian, Seychelles, Mozambican, and French institutions. All au- 33 thors edited, read, and approved the final manuscript. 34 35 Abstract 36 Bats provide key ecosystem services such as crop pest regulation, pollination, seed dispersal, 37 and soil fertilization. Bats are also major hosts for biological agents responsible for zoonoses, 38 such as coronaviruses (CoVs). The islands of the Western Indian Ocean are identified as a major 39 biodiversity hotspot, with more than 50 bat species. In this study, we tested 1,013 bats belonging 40 to 36 species from Mozambique, Madagascar, Mauritius, Mayotte, Reunion Island and Sey- 41 chelles, based on molecular screening and partial sequencing of the RNA-dependent RNA pol- 42 ymerase gene. In total, 88 bats (8.7%) tested positive for coronaviruses, with higher prevalence 43 in Mozambican bats (20.5% ± 4.9%) as compared to those sampled on islands (4.5% ± 1.5%). 44 Phylogenetic analyses revealed a large diversity of α- and β-CoVs and a strong signal of co- 45 evolution between CoVs and their bat host species, with limited evidence for host-switching, 46 except for bat species sharing day roost sites. 47 48 Importance 2 bioRxiv preprint doi: https://doi.org/10.1101/742866; this version posted March 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 This is the first study to report the presence of coronaviruses (CoVs) in bats in Mayotte, 50 Mozambique and Reunion Island, and in insectivorous bats in Madagascar. Eight percent of the 51 tested bats were positive for CoVs, with higher prevalence in continental Africa than on islands. 52 A high genetic diversity of α- and β-CoVs was found, with strong association between bat host 53 and virus phylogenies, supporting a long history of co-evolution between bats and their associ- 54 ated CoVs in the Western Indian Ocean. These results highlight that strong variation between 55 islands does exist and is associated with the composition of the bat species community on each 56 island. Future studies should investigate whether CoVs detected in these bats have a potential 57 for spillover in other hosts. 58 59 60 61 Keywords: bat, coronavirus, islands, tropical, evolution, ecology 3 bioRxiv preprint doi: https://doi.org/10.1101/742866; this version posted March 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 62 Text – 3158 words 63 Introduction 64 The burden of emerging infectious diseases has significantly increased over the last decades 65 and is recognized as a major global health concern. In 2018, the World Health Organization 66 (WHO) established the “Blueprint priority disease list”, identifying viruses such as Ebola, Lassa 67 fever, Middle East Respiratory Syndrome (MERS), and Nipah fever as significant threats to 68 international biosecurity 1. This list also highlights the potential pandemic risk from the emer- 69 gence of currently unknown zoonotic pathogens, collectively referring to these unknown threats 70 as “disease X” 1. Investigation of the potential zoonotic pathogens in wild animals, particularly 71 vertebrates, is thus critical for emerging infectious disease preparedness and responses. 72 Bats represent nearly 1,400 species and live on all continents except Antarctica 2. They 73 provide key ecosystem services such as crop pest regulation, pollination, seed dispersal, and 74 soil fertilization 3–10. Bats are also recognized as reservoirs of many zoonotic pathogens, includ- 75 ing coronaviruses (CoVs) 11–13. Indeed, several CoVs originating from bats have emerged in 76 humans and livestock with sometimes major impacts to public health. For instance, in 2003, the 77 Severe Acute Respiratory Syndrome (SARS) CoV emerged in humans, after spillover from bats 78 to civets14–18, and led to the infection of 8,096 people and 774 deaths in less than a year 19. 79 Our study area spans geographic locations across the islands of the Western Indian 80 Ocean and southeastern continental Africa (SECA) (Figure 1). These islands have diverse ge- 81 ological origins that have influenced the process of bat colonization and species distributions 82 20. The ecological settings and species diversity on these islands for bats are notably different. 83 On Madagascar, more than 45 bat species are known to occur, of which more than 80 % are 84 endemic to the island 21–23. The smaller studied islands of the Western Indian Ocean, Mauritius, 85 Mayotte, Reunion Island, and Mahé (Seychelles), host reduced bat species diversity (e.g. three 4 bioRxiv preprint doi: https://doi.org/10.1101/742866; this version posted March 17, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 86 species on Reunion Island), whereas SECA supports a wide range of bat species. To date, sev- 87 eral studies have identified bat-infecting CoVs in countries of continental Africa, including 88 Zimbabwe 24, South Africa 25,26, Namibia 27, and Kenya 28,29. CoVs have also been reported in 89 fruit bats (Pteropodidae) in Madagascar, where β-coronaviruses belonging to the D-subgroup 90 were identified in Eidolon dupreanum and Pteropus rufus 30. 91 In this study, we investigated the presence of CoVs in over 1,000 individual bats be- 92 longing to 36 species, sampled on five islands (Madagascar, Mauritius, Mayotte, Reunion Is- 93 land, and Mahé) and one continental area (Mozambique). Based on molecular screening and 94 partial sequencing of the RNA-dependent RNA polymerase gene, we (i) estimated CoV preva- 95 lence in the regional bat populations, (ii) assessed CoV genetic diversity, and (iii) identified 96 associations between bat families and CoVs, as well as potential evolutionary drivers leading 97 to these associations. 98 99 Results 100 Prevalence of CoV 101 A total of 1,013 bats were tested from Mozambique, Mayotte, Reunion Island, Sey- 102 chelles, Mauritius and Madagascar (Figure 1). In total, 88 of the 1,013 bat samples tested pos- 103 itive for CoV by Real-Time PCR (mean detection rate: 8.7%). The prevalence of positive bats 104 was different according to the sampling locations (χ² = 77.0, df = 5; p<0.001), with a higher 105 prevalence in Mozambique (± 95% confidence interval: 20.5% ± 4.9%) than on all Western 106 Indian Ocean islands (4.5% ± 1.5%) (Figure 2). A significant difference in the prevalence of 107 positive bats was also detected between families (χ² = 44.8, df = 8; p<0.001; Supplementary 108 Figure S1).
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